The evolutionary developmental biology of tinkering: an introduction to the challenge

Abstract

Recent developments in evolutionary biology have conflicting implications for our understanding of the developmental bases of microevolutionary processes. On the one hand, Darwinian theory predicts that evolution occurs mostly gradually and incrementally through selection on small-scale, heritable changes in phenotype within populations. On the other hand, many discoveries in evolutionary developmental biology--quite a few based on comparisons of distantly related model organisms--suggest that relatively simple transformations of developmental pathways can lead to dramatic, rapid change in phenotype. Here I review the history of and bases for gradualist versus punctuationalist views from a developmental perspective, and propose a framework with which to reconcile them. Notably, while tinkering with developmental pathways can underlie large-scale transformations in body plan, the phenotypic effect of these changes is often modulated by the complexity of the genetic and epigenetic contexts in which they develop. Thus the phenotypic effects of mutations of potentially large effect can manifest themselves rapidly, but they are more likely to emerge more incrementally over evolutionary time via transitional forms as natural selection within populations acts on their expression. To test these hypotheses, and to better understand how developmental shifts underlie microevolutionary change, future research needs to be directed at understanding how complex developmental networks, both genetic and epigenetic, structure the phenotypic effects of particular mutations within populations of organisms.